Slow life-history strategies are associated with negligible actuarial senescence in western Palaearctic salamanders

Abstract

Actuarial senescence has been viewed for a long time as an inevitable and uniform process. However, the work on senescence has mainly focused on endotherms with deterministic growth and low regeneration capacity during the adult stage, leading to a strong taxonomic bias in the study of ageing. Recent studies have highlighted that senescence could indeed display highly variable trajectories that correlate with species life-history traits. Slow life histories and indeterminate growth seem to be associated with weak and late senescence. Furthermore, high regenerative abilities could lead to negligible senescence in ectotherms. However, demographic data for species that would allow testing of these hypotheses are scarce. Here, we investigated senescence patterns in ‘true salamanders’ from the western Palaearctic. Our results showed that salamanders have slow life histories and that they experience negligible senescence. This pattern was consistent at both intra- and interspecific levels, suggesting that the absence of senescence may be a phylogenetically conserved trait. The regenerative capacities of salamanders, in combination with other physiological and developmental features such as an indeterminate growth and a low metabolic rate, probably explain why these small ectotherms have lifespans similar to that of large endotherms and, in contrast with most amniotes, undergo negligible senescence. Our study seriously challenges the idea that senescence is a ubiquitous phenomenon in the tree of life.

Population position along the fast–slow life‐history continuum predicts intraspecific variation in actuarial senescence

“…included anurans and salamanders in their comparative analyses and found a great diversity in patterns of actuarial senescence among the four species that were studied. In contrast,Cayuela, Olgun, et al (2019) highlighted the absence of actuarial senescence in three species of salamanders from western…”

“…Although a few case studies on free-ranging populations failed to detect any increase in mortality rate with age (Cayuela, Olgun, et al, 2019;Jones et al, 2014), most recent syntheses revealed two major facts. First, actuarial senescence is a nearly ubiquitous process in the living world (Nussey, Froy, Lemaitre, Gaillard, & Austad, 2013;Shefferson, Jones, & Salguero-Gómez, 2017).…”

“…Most of the studies on senescence in vertebrates focus on endothermic organisms, such as birds and mammals, and largely neglect ectotherms (Bronikowski et al, 2002;Hoekstra, Schwartz, Sparkman, Miller, & Bronikowski, 2019;Jones et al, 2014;Lemaître et al, 2015; but see Cayuela, Akani, et al, 2019;Cayuela, Olgun, et al, 2019;Massot et al, 2011;Sparkman, Arnold, & Bronikowski, 2007;Warner, Miller, Bronikowski, & Janzen, 2016). Both actuarial and reproductive senescence are understudied in ectotherms, mainly due to the scarcity of demographic data and methodological limitations (juveniles cannot be marked easily and information about the age of individuals is often partial and uncertain).…”

Salamander Insights Into Ageing and Rejuvenation

“…While the underlying basis of their exceptional longevity remains unknown, salamanders exhibit an uncommon resistance to ageing. Although few studies have addressed this topic, these, together with evidence from captive records in zoos and laboratories, suggest that a number of urodele species do not display the traditional signs of physiological decay that accompany mammalian ageing and are thus considered organisms of "negligible senescence" (Finch, 1990;Margotta et al, 2002;Cayuela et al, 2019). This phenomenon, also observed in other vertebrates such as turtles, rockfish and naked mole rats (Finch, 2009), is intrinsically linked to a defiance of the Gompertz-Makeham law of mortality (Gompertz, 1825;Makeham, 1860), which states that death risk increases exponentially as an organism ages.…”

“…This phenomenon, also observed in other vertebrates such as turtles, rockfish and naked mole rats ( Finch, 2009 ), is intrinsically linked to a defiance of the Gompertz-Makeham law of mortality ( Gompertz, 1825 ; Makeham, 1860 ), which states that death risk increases exponentially as an organism ages. Indeed, a recent study involving three salamander species ( Lyciasalamandra fazilae, Salamandra salamandra , and Salamandra perspicillata ), indicates that their mortality rate is stable and weakly affected by age, in keeping with them exhibiting negligible senescence ( Cayuela et al, 2019 ). This observation raises several important yet outstanding questions, including whether salamanders manifest cellular hallmarks of ageing as defined in mammalian contexts ( Lopez-Otin et al, 2013 ), whether they age at the molecular level, what principles govern ageing—or lack of — in these organisms and, in particular, what is the role played by their extreme regenerative abilities in this process.…”